Climate change effects on thermal tolerance plasticity and population dynamics in the eelgrass sea hare, Phyllaplysia taylori By Richelle Li Tanner A dissertation submitted in partial satisfaction of the requirements for the degree of Doctor of Philosophy in Integrative Biology in the Graduate Division of the University of California, Berkeley Committee in charge: Professor Jonathon H. Stillman, Co-Chair Professor Wayne P. Sousa, Co-Chair Professor Caroline M. Williams Professor Mark T. Stacey Spring 2018 1 Climate change effects on thermal tolerance plasticity and population dynamics in the eelgrass sea hare, Phyllaplysia taylori © 2018 by Richelle Tanner 2 Abstract Climate change effects on thermal tolerance plasticity and population dynamics in the eelgrass sea hare, Phyllaplysia taylori By Richelle Li Tanner Doctor of Philosophy in Integrative Biology Professors Jonathon H. Stillman & Wayne P. Sousa, Co-Chairs Understanding how climate change affects the physiology and population dynamics of grazers that can reduce epiphyte growth on seagrass is important for predicting the future dynamics of seagrass ecosystems. Seagrass habitats provide a number of important ecosystem services, including carbon sequestration, nutrient mitigation, sedimentation and erosion control, and providing nursery habitat for fishes and invertebrates. Climate change threatens seagrass communities as increased temperature promotes photosynthesis-inhibiting epiphytic growth. Grazers have the potential to mitigate this increased epiphytic growth if their physiological performance is maintained in future climatic regimes. Phyllaplysia taylori is a grazing sea hare with two generations per year in the Zostera marina seagrass habitat along the Pacific coast of North America. It exhibits direct embryonic development with crawl-away young, greatly limiting long-distance dispersal capacity and population connectivity. In Central CA, P. taylori is a bivoltine species with non-overlapping generations that span different seasonal regimes. As a grazer species inhabiting many thermally disparate environments throughout space and time, it provides an opportunity to look at how physiological plasticity plays a role in population persistence and how this can impact the seagrass ecosystem. In my dissertation, I examined the factors that influence P. taylori’s geographic distribution at different spatial scales and variation in the plasticity of thermal physiology across life stages and among populations. In my first chapter, I documented where P. taylori populations are found along the coast and investigated the environmental and/or ecological factors that account for their distribution. Although temperature was expected to be a major driver of population persistence, this was not the case. Nutrient-rich runoff from anthropogenically-modified land was the strongest predictor of P. taylori presence, as it may contribute to epiphyte growth resulting in increased sea hare food availability. I also found that seasonal fluctuations in eelgrass density and length, epiphytic coverage, and average temperature played the biggest roles in determining relative seasonal abundance of P. taylori. The presence/absence models applied to existing restoration sites within San Francisco Bay indicated a 53% success rate for P. taylori within currently planned restoration areas. These correlation models demonstrate that it is important to consider grazer communities when planning restoration efforts. In my second chapter, I investigated the physiological differences among the populations examined in Chapter 1, testing for a relationship between phenotypes and thermal characteristics 1 of the source habitat. To address intraspecific differences in thermal tolerance plasticity across their geographic range, thermal sensitivity of metabolic rate and upper critical limits (CTmax), as well as the acclimation response of these metrics were assessed. Metabolic rate estimated by whole-organism respiration rate showed depression after acute heat stress in populations with warm thermal habitat histories. This trend was only observed in lab acclimation groups above 17ºC and indicates beneficial acclimation, whereby acclimation to warmer temperatures dampens the acute heat stress response, resulting in less energy expenditure with stress. Compared with other taxa, P. taylori had high intraspecific variation in CTmax. Short-term plasticity of CTmax with acclimation varied among collection sites, but contrary to my prediction, was not correlated with microhabitat temperature regimes. Instead, short-term plasticity elevated CTmax and its acclimation capacity well above habitat temperatures in no apparent pattern. Therefore, this study does not find sufficient evidence for positive selection acting upon the plasticity of CTmax. However, on the scale of seasons within a single population, I found significant seasonal acclimatization whereby individuals collected in the summer exhibited the highest CTmax and the greatest capacity for acclimation in this trait. These data provided relevant information on season-specific phenotypes, which were investigated in the next chapter. In my third chapter, I used laboratory acclimation temperature treatments to induce seasonally-relevant phenotypes. Within these temperature treatments, I investigated how shifts in transgenerational and developmental plasticity impacted offspring success. I found that seasonally-driven differences in offspring success were correlated with egg size and total maternal investment per clutch (transgenerational plasticity), with winter temperatures corresponding to larger, fewer eggs. Future summer temperatures resulted in significantly decreased total maternal investment with more investment per egg. Developmental plasticity sufficiently mitigated differences in maternal investment in the current climatic regime to result in equal numbers of successful offspring in all seasonal scenarios, but acclimation capacity and offspring success decreased with acute and chronic heat stress in mothers and offspring. Transgenerational and developmental plasticity decrease with high temperatures, suggesting that these life stages may be more susceptible and subject to selection with increased habitat temperature. These studies illustrate how the physiology of an important grazer in the eelgrass ecosystem will respond to climate change and outlines potential consequences at the population level. Although short-term plasticity sufficiently buffers adults from future climate shifts, maturation is made difficult by inadequate transgenerational and developmental plastic responses. While some populations may suffer due to increased mean and variation of habitat temperatures, responses across populations are highly variable. Therefore, in restoration efforts, selection of relevant source populations of P. taylori based on thermal physiology is highly advantageous. Understanding how the physiological plasticity of P. taylori is able to compensate for future climatic shifts is important for both eelgrass restoration and in determining how physiologically-plastic taxa cope with fluctuating environments. 2 Dedication To my sister, Julia. i Table of Contents Abstract……………………………………………………………………………………..……..1 Dedication……………………………………………………………………...………………….i Table of contents…………………………………………………………………...…….….……ii Acknowledgements………………………………………………………………………………iii Chapter 1…………………………………………………………………………………………..1 Predicting Phyllaplysia taylori (Anaspidea: Aplysiidae) presence from land use in Northeastern Pacific estuaries for use in the eelgrass restoration framework Chapter 2………...…………………………………………………………………………….....27 Intraspecific variation in thermal tolerance and temperature sensitivity of respiration rate in the eelgrass sea hare, Phyllaplysia taylori, along the Pacific coast of the United States Chapter 3…………………………………………………………………………………………49 Reduced transgenerational thermal tolerance plasticity in direct developer Phyllaplysia taylori with climate change ii Acknowledgements This work would not have been possible without the support of people throughout my life who guided, assisted, and encouraged me to become a better scientist. First and foremost, I am grateful to Jonathon Stillman and Wayne Sousa for taking the chance on interviewing me for a graduate position. My development as a scientist at Berkeley would not have been possible without their support of my ideas and their guiding wisdom. They have shown me the importance of developing ideas that bridge multiple disciplines and I am grateful that they encouraged me to be inclusive of themes in physiology, ecology, and even topics beyond their expertise in my research. Even before arriving at Berkeley, my undergraduate advisors Dave Ginsburg and Lisa Collins were fundamental in fostering my ambitions and providing the support needed for me to move forward. I am so grateful for their continued support throughout the last seven years at both USC and Berkeley; I would have never imagined the relationship we would continue to have after my undergraduate education and I look forward to many more years of friendship. I would like to thank my committee members Caroline Williams and Mark Stacey for broadening my horizons and guiding my ideas over the last three years. Taking Caroline’s physiology course completely remodeled my framework of thinking for my dissertation, and it has been a pleasure learning from her. Every time I walk away from a meeting with her, I simultaneously feel inspired and like there was still